Deep Brain Stimulation Target Selection for Parkinson's Disease
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REVIEW ARTICLE COPYRIGHT © 2016 THE CANADIAN JOURNAL OF NEUROLOGICAL SCIENCES INC.
Deep Brain Stimulation Target Selection
for Parkinson’s Disease
Christopher R. Honey, Clement Hamani, Suneil K. Kalia, Tejas Sankar, Marina
Picillo, Renato P. Munhoz, Alfonso Fasano, Michel Panisset
ABSTRACT: During the “DBS Canada Day” symposium held in Toronto July 4-5, 2014, the scientific committee invited experts
to discuss three main questions on target selection for deep brain stimulation (DBS) of patients with Parkinson’s disease (PD). First, is the
subthalamic nucleus (STN) or the globus pallidus internus (GPi) the ideal target? In summary, both targets are equally effective
in improving the motor symptoms of PD. STN allows a greater medications reduction, while GPi exerts a direct antidyskinetic effect.
Second, are there further potential targets? Ventral intermediate nucleus DBS has significant long-term benefit for tremor control but
insufficiently addresses other motor features of PD. DBS in the posterior subthalamic area also reduces tremor. The pedunculopontine
nucleus remains an investigational target. Third, should DBS for PD be performed unilaterally, bilaterally or staged? Unilateral STN DBS
can be proposed to asymmetric patients. There is no evidence that a staged bilateral approach reduces the incidence of DBS-related
adverse events.
RÉSUMÉ: Choix de cible en matière de stimulation cérébrale profonde dans le cas de la maladie de Parkinson. C’est durant le symposium
« Stimulation cérébrale profonde (SCP)-Fête du Canada » tenu à Toronto les 4 et 5 juillet 2014 qu’un comité scientifique a invité des experts à aborder trois
questions fondamentales en ce qui regarde le choix de cible en matière de SCP dans le cas de patients atteints de la maladie de Parkinson (MP).
Premièrement, il leur a été demandé si le noyau sous-thalamique (NST) ou le globus pallidus interne (GPi) constituaient une cible idéale. En résumé, il a été
établi que ces deux cibles s’équivalent quant à la capacité d’atténuer les symptômes moteurs de la MP. À ce sujet, si le NST permet une réduction plus
importante de la consommation de médicaments, le GPi, lui, exerce un effet anti-dyskinétique direct. Deuxièmement, on a demandé aux experts dans quelle
mesure il pouvait y avoir d’autres cibles potentielles. Ainsi, bien que la SCP du noyau ventral intermédiaire procure un avantage important à long terme, elle
demeure une avenue insuffisante en ce qui a trait aux autres aspects moteurs de la MP. Soulignons que la SCP de la région sous-thalamique postérieure
contribue aussi à réduire les tremblements. Quant au noyau pédonculopontin, il demeure une piste de recherche à explorer. Enfin, est-ce que la SCP devrait
être effectuée de façon unilatérale, bilatérale ou être échelonnée en ce qui a trait à des cas de MP ? La SCP unilatérale du NST peut être proposée à des
patients dont la symptomatologie est asymétrique. De plus, aucune preuve ne permet de conclure qu’une stimulation bilatérale échelonnée entraîne une
réduction de la fréquence des manifestations indésirables liées à la SCP.
Keywords: deep brain stimulation, globus pallidus internus, movement disorder, movement disorder surgery, Parkinson’s disease,
subthalamic nucleus, surgical target, ventral intermediate nucleus
doi:10.1017/cjn.2016.22 Can J Neurol Sci. 2017; 44: 3-8
During the “DBS Canada Day” symposium held in Toronto in PD? Third, should DBS for PD be performed unilaterally,
July 4-5, 2014, the scientific committee invited experts to share bilaterally or staged?
their knowledge of target selection for deep brain stimulation These are the questions facing functional neurosurgeons in
(DBS) of patients with Parkinson’s disease (PD). Experts were Canada on a daily basis. This paper attempts to distill the current
provided with selected topics for which they were asked to literature in this area into a succinct summary of what is known,
summarize the current literature and highlight what was known what is often done, and what needs to be studied. This summary
and what was still controversial within the field. The topics were will be of interest for both surgeons new to the field and for
divided into three questions. First, is the subthalamic nucleus non-surgeons who may wonder what controversies are facing
(STN) or the globus pallidus internus (GPi) the ideal target for their surgical colleagues. Our surgical colleagues may find this a
DBS in PD? Second, are there other potential targets for DBS timely reference, highlighting what needs to be explored in our
From the Division of Neurosurgery (CRH), University of British Columbia, Vancouver, British Columbia; Research Imaging Centre (CH), Centre for Addiction and Mental Health, Toronto;
Department of Surgery (CH, SKK), Division of Neurosurgery, University of Toronto; Morton and Gloria Shulman Movement Disorders Centre and the Edmond J. Safra Program in Parkinson’s
Disease (MP,RPM, AF), Toronto Western Hospital, University Health Network, Toronto, Ontario; Division of Neurosurgery (TS), Walter C. MacKenzie Health Sciences Centre, University
of Alberta, Edmonton, Alberta; Division of Neurology (MP), Department of Medicine, Hôpital Notre-Dame, University of Montreal Health Centre, Montréal, Québec, Canada; Centre for
Neurodegenerative Diseases (CEMAND) (MP), Neuroscience Section, Department of Medicine and Surgery, University of Salerno, Salerno, Italy.
RECEIVED AUGUST 25, 2015. FINAL REVISIONS SUBMITTED JANUARY 20, 2016.
Correspondence to: Christopher R. Honey, Associate Professor of Neurosurgery, University of British Columbia, 8105-2775 Laurel St., Vancouver, BC, Canada V5Z 1M9. Email:
chris.honey@telus.net
THE CANADIAN JOURNAL OF NEUROLOGICAL SCIENCES 3
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field and how tenuous the bases for some of our current ARE THERE OTHER POTENTIAL TARGETS FOR DBS IN
practices are. PARKINSON’S DISEASE?
The original symposium was sponsored by Medtronic (conflict The ventral intermediate nucleus (Vim) of the thalamus has
of interest detailed below). The final report has no industry always been a surgical target for patients with PD and continues to
specific recommendations and was carefully screened to avoid be an option for tremor-dominant patients. More recently,
any potential bias. some centres have presented data suggesting that the posterior
subthalamic area (PSA) and pedunculopontine nucleus (PPN)
IS THE STN OR THE GPI THE IDEAL TARGET FOR DBS IN may address certain symptoms of PD that are refractory to DBS
PARKINSON’S DISEASE? in the more common areas. Each of these three targets is
discussed below.
The ideal DBS target for the treatment of PD remains
controversial. High frequency stimulation in either the STN or GPi
has been shown to improve the motor symptoms of the disease.1 Ventral intermediate nucleus (Vim) of thalamus
A comparison of the benefits of stimulating STN versus GPi has Deep brain stimulation targeting the Vim was introduced as one
been carried out in different studies.2-11 Initial randomized 2,5 and of the original targets for tremor in PD.19-21 Since the early nineties,
non-randomized trials (e.g. conducted by the DBS study group)3 Vim has been the target of choice for the surgical treatment of
comparing these targets showed no major differences in efficacy. medically refractory essential tremor by DBS.22-26 Compared with
These same results have been largely replicated in follow-up studies other contemporary DBS targets (ie. STN or GPi) the Vim cannot
published by the DBS study group at three to six years after currently be visualized on pre-op magnetic resonance imaging (MRI)
surgery,6,10 but not in some open label reports.4 To help address for target planning. As such, many centres employ targeting
controversial aspects of target selection, randomized controlled trials paradigms based on a variety of indirect approaches combined
with blinded scoring have been designed.9,11 In particular, the with microelectrode recordings, intra-operative macrostimulation
Veterans-Affairs study included 299 PD patents randomized to and intra-operative clinical assessments. By this combined
receive DBS in either target.9 No significant differences in efficacy multimodal approach the DBS lead can be positioned within the Vim
were found between patients receiving GPi or STN DBS.9 The maximizing the potential for therapeutic benefit and minimizing
primary outcome was the change in motor function, as blindly thresholds for off-target side effects. The current evidence for Vim
assessed on the Unified Parkinson’s Disease Rating Scale, part III DBS in PD has been recently reviewed.27-30 Long-term Vim DBS
(UPDRS-III), while patients were receiving stimulation but not has a significant benefit for tremor control but insufficiently
receiving antiparkinsonian medication. Secondary outcomes addresses other key motor features of PD. While contralateral
included self-reported function, quality of life, neurocognitive tremor benefits greater than 80% can be sustained over five years in
function, and adverse events. In summary, most evidence published well selected patients, 23,24,29,31-33 in general there is no
to date has shown that DBS in either the STN or GPi is equally improvement in UPDRS III scores, rigidity, akinesia or postural
effective in improving the motor symptoms of Parkinson’s disease. instability.31,23,24,29 In those patients who lose anti-tremor benefit
One of the major drivers for recent trials of GPi DBS was the with time it is not clear if this is due to adaptation, progression of PD
recognition of psychiatric complications after STN stimulation or a combination of both.
(e.g. depression, hypomania, and suicide, among others).12-16 As Ventral intermediate nucleus DBS may currently be
in most studies on efficacy, those with a blinded design showed no considered in patients with tremor-dominant PD with an
statistically significant differences in the rate of psychiatric associated slow disease progression. If the patient’s other
complications between targets,18,9 though there did appear to be symptoms of PD are a significant source of disability at the time of
trend toward a somewhat higher incidence with STN DBS. To surgery, the multidisciplinary surgical team should consider STN
date, the only consensus in the field is that STN DBS increases the or GPi DBS upfront. Consideration can be made of a second target
postoperative risk of verbal fluency deficits.12,14,16 These verbal in a delayed fashion (i.e. STN or GPi DBS after initial Vim DBS
deficits are typically detected by neuropsychologists using a or vice versa), as the symptoms progress. If optimal tremor control
battery of tests including the Controlled Oral Word Association is not achieved and/or sustained in those patients with STN or GPi
Test (COWAT) but, in our experience, are rarely a concern for the DBS upfront, subsequent contralateral Vim DBS is an option.
patient or their family.
As clinical trials have suggested that both targets are effective
in treating the motor symptoms of PD, one may ask whether there Posterior subthalamic area (PSA)
are any selected symptoms that may favor the use of one The PSA has a variable definition, which may include the zona
target over the other. Subthalamic DBS allows a meaningful incerta (Zi), prelemniscal radiations (Raprl) and/or the area just
reduction in dopaminergic medication in the post-operative phase, lateral to the rostral-most portion of the red nucleus.34 To date
which typically cannot be achieved with GPi stimulation.9 there is no consensus on specific target planning for the PSA;
Consequently, when one of the goals of the surgery is to reduce rather, an indirect approach is used to target the general area
medication intake (e.g., to improve dopamine dysregulation posterior to the STN and lateral to the red nucleus. Recently the
syndrome or hyperdopaminergic symptoms such as hallucinations use of PSA DBS has been reviewed by Blomstedt and
and hypomania), the STN may be a better target. When a direct colleagues34 and reports in the literature demonstrate a consistent
antidyskinetic effect is desired, the GPi may be a better option in tremor reduction in PD as well as essential tremor and tremor
patients who do not need medication reduction.17 In patients with related to multiple sclerosis. A subset of small, retrospective,
cognitive and psychiatric symptoms, some centers may favour the non-randomized studies suggest that PSA may provide better
GPi over the STN.18 tremor control compared to Vim and STN DBS.34-37 One group
4
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has retrospectively shown that PD patients had more improvement bilateral procedure; and 4) the stimulation-related side effects of
in UPDRS III motor scores with stimulation in the PSA region bilateral DBS may be more severe than unilateral DBS.47,48 A few
compared to an earlier cohort receiving stimulation within the centres now routinely choose to perform unilateral DBS at initial
STN nucleus.36 implantation, followed by staged implantation of a contralateral
At this time no firm recommendations for PSA DBS can be lead at a later date.47,49 The immediate problem of this approach
made. It may be considered for tremor-dominant PD as discussed for the patient is that it requires two visits to the operating room
above for Vim DBS with the possible advantage of also with two stereotactic frame applications.
improving other symptoms of PD. Electrode placement may be At the opposite end of the spectrum, some authors have
planned such that the dorsal contacts are in the Vim and the suggested that there may be potential benefit from stimulation
ventral contacts are in the PSA which may allow for more directed to multiple targets simultaneously (i.e., through leads
programming options. implanted bilaterally into both the GPi and STN in the same
patient). The multiple-target approach has been justified on the
Pedunculopontine nucleus basis of a potential synergistic effect during stimulation at
different nodes within the basal ganglia50,51 or, when applied in a
Postural instability is a significant issue for many patients with
staged fashion, as a means of rescuing the loss of therapeutic
PD. Importantly it can contribute to falling which can lead to
effect from stimulation at the initial target.52
significant injury and hospitalization (e.g., hip fracture).
There has so far been no prospective, randomized,
Unfortunately this PD symptom is generally refractory to medical
blinded-assessment trial comparing unilateral DBS to best
management and contemporary “classical” surgical targets
medical management in PD. However, class II data from the
including STN and GPi DBS. Therefore the PPN, a brainstem
COMPARE trial18 suggest that unilateral STN or GPi DBS both
relay centre that plays a role in locomotion, has been targeted for
result in a significant improvement in motor scores as measured
DBS in investigational studies. The PPN is a predominantly
using the UPDRS-III. Several case series report that while the
cholinergic nucleus located posteriorly and caudally to the
motor effects of unilateral DBS are more significant contralateral
substantia nigra pars compacta (SNpc) extending to the level of
to the stimulated side, ipsilateral motor improvement is also
the locus coeruleus. It receives input from the basal ganglia (STN
observed following both STN53-58 and GPi59 stimulation.
and GPi) and has output to multiple subcortical targets including
Ipsilateral motor benefit seems to be unrelated to which
the thalamus and striatum in addition to targets within the brain-
hemisphere is targeted59 and, while the underlying mechanism is
stem and spinal cord.38-40 For the purposes of targeting it is
uncertain, a single imaging study using positron emission
important to note that there is some variability between
tomography (PET) points to deactivation of the contralateral
institutions and as such no formal consensus for PPN DBS has
pallidum as a possible explanation.60 As for non-motor effects, the
been established. To date, only a handful of centres worldwide
COMPARE trial showed that mood may be improved either by
have published their experience with PPN DBS.39-45 There is
unilateral STN or GPi DBS, while—and in line with the bilateral
significant variability in both targeting (i.e., unilateral vs. bilateral
DBS literature—unilateral STN stimulation results in verbal
DBS, and multi-target DBS) and patient selection (i.e., those
fluency impairment.61,63 That being said, verbal fluency may be
patients with dominant gait instability versus those that would be
more profoundly impaired following bilateral compared to
ideal candidates for STN or GPi DBS). The reported number of
unilateral STN stimulation.64
patients studied in the literature is small and there is a trend that
To date, there has been no prospective, randomized study
PPN DBS, often at lower frequencies and in combination with
directly comparing staged bilateral DBS to upfront bilateral DBS
STN, may provide improvements in reported number of falls and
in PD. The existing data on staged DBS come exclusively from
freezing of gait. However with blinded DBS on/off evaluation of
observational cohort studies in which unilateral DBS patients go
UPDRS III no objective improvement has been documented.43,46
on to have the contralateral side implanted; consequently, they are
Given the current evidence, no firm recommendations can be
confounded by selection bias. With this in mind, Tanei et al.64
made at this time and PPN DBS remains an investigational target.
found that overall motor improvement measured with the
Further study is necessary to address appropriate patient selection,
UPDRS-III was similar in both bilateral and staged bilateral
anatomical target selection, the role of combined targets and
groups. Additionally, both a follow-up analysis of the COMPARE
programming parameters.
cohort65 and a single centre study by Sung et al.,49 found that
the single best predictor of early staged implantation of the
SHOULD DBS FOR PD BE PERFORMED UNILATERALLY, contralateral side was greater asymmetry in motor PD symptoms
BILATERALLY OR STAGED? at baseline. There is no convincing evidence so far that a staged
In the vast majority of centres, PD patients who are suitable bilateral approach is safer or reduces the overall incidence of
candidates for DBS are treated with upfront, bilateral stimulation DBS-related adverse events.
of either the STN or GPi.13 Many centres opted for bilateral STN Simultaneous, upfront implantation and stimulation of both the
DBS because the reduced dopaminergic medication following STN and GPi has been described by a single group.50,51 The
unilateral stimulation often exacerbated the contralateral authors found some evidence for a synergistic motor effect with
symptoms and could worsen gait.28 More recently, there has been two-target stimulation but these results have not yet been repli-
some interest in unilateral targeting.47 Potentially compelling cated, possibly due to the unwillingness of many centres to accept
reasons to consider unilateral DBS include: 1) PD is an the increased surgical time and risk that may be incurred by the
asymmetrical disease; 2) unilateral pallidotomy has long been implantation of four (instead of the usual two) DBS leads. By
known to produce some bilateral benefits in PD;48 3) the surgical contrast, several groups have reported on their experience with
risks of unilateral implantation may be reduced compared to a “rescue” DBS to recover lost therapeutic efficacy in patients
Volume 44, No. 1 – January 2017 5
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following an initial period—typically several years—of good The scientific committee (CRH, RPM, AF and MP) selected
motor response to DBS. Successful rescue of motor benefit has three Canadian neurosurgeons (CH, SKK and TS) to share their
been achieved both with bilateral STN DBS following initial GPi knowledge of target selection for deep brain stimulation (DBS) of
implantation4,66-68 and with bilateral GPi DBS following initial patients with Parkinson’s disease (PD) and asked them to focus
STN implantation.52,69 However, there are insufficient data to their discussion around the three controversial questions that
conclude whether two-site stimulation in the rescue setting is currently face our field.
actually synergistic, or whether stimulation at the initial target can
be turned off once rescue target stimulation begins. DISCLOSURES
The absence of data from prospective, randomized,
blinded-assessment trials points the way to future directions in the Marina Picillo has the following disclosures: MJFF, Grant
evaluation and implementation of unilateral, staged, and multiple- recipient, Grant; UHN, Salary, Employee; University of Salerno,
target strategies for DBS in PD. Though limited available Salary, Employee.
evidence suggests that unilateral DBS at either the STN or GPi Tejas Sankar has the following disclosures: University of
leads to significant motor improvement in PD, hard data from a Alberta, Principal investigator, Research support/grant; Weston
randomized trial comparing unilateral DBS to best medical Foundation, Co-investigator, Research support/grant.
management are lacking. Such data would critically help to Alfonso Fasano has the following disclosures: Abbvie,
clarify the risk-benefit balance for unilateral DBS. Similarly, a Consultant/Advisor, Honoraria/Consulting fee; Boston Scientific,
randomized trial of staged bilateral versus upfront bilateral DBS Consultant/Advisor, Honoraria/Consulting fee; Medtronic,
would help to answer the question of whether staging may be safer Consultant/Advisor, Honoraria, Consulting fees, Research support;
for patients, and whether there exists a subset of PD patients who TEVA Canada, Consultant/Advisor, Honoraria; Novartis,
may be ideally suited for staging. Finally, additional work is Consultant/Advisor, Honoraria; UCB Pharma, Consultant/Advisor,
required to elucidate whether there is a true synergistic effect Honoraria.
when the STN and GPi are stimulated simultaneously, and to what Clement Hamani has the following disclosures: St. Jude Medical,
degree this may be clinically relevant in patients with PD. Consultant, Consulting fees.
Christopher Honey has the following disclosures: Medtronic,
CONCLUSION Speaker, Honoraria; Medtronic, Consultant, Consulting fees.
Suneil Kalia, Renato Puppi Munhoz and M. Panisset do not
There is no universal consensus on the ideal target for DBS in
have anything to disclose.
patients with Parkinson’s disease. Most prospective randomized
studies have shown that patients with STN DBS had a similar
clinical improvement compared to those with GPi DBS. If there
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